978–0–19–969257–6 04-Royle-c04-drv Royle-et-al (Typeset by SPi, Chennai) 62 of 347 March 31, 2012 14:59 OUP UNCORRECTED PROOF – REVISES, 31/3/2012, SPi CHAPTER 4 Patterns of parental care in vertebrates Sigal Balshine 4.1 Introduction reproductive success. However, parental care also has three potential costs: 1) a decrease in parental Understanding parental care behaviour has survival, 2) decreased growth and associated fecun- remained a core research area in evolutionary dity reduction, and 3) fewer remating opportu- behavioural ecology. Why the fascination with nities (Gross and Sargent 1985). Scientists have parental behaviour? Many human cultures have used these costs and benefits to better understand a strong focus on children and parenting and our when care will evolve and which sex will provide extensive and prolonged care for our own young care (Maynard-Smith 1977; Balshine-Earn and Earn undoubtedly contributes to our fascination with 1997; Houston et al. 2005). Vertebrate groups that parental care in other animals. Also by studying show great variation in care types, like teleost fishes parental care, behavioural scientists can gain a and shorebirds, have been particular useful models useful window on the social dynamics of family in the search for a better understanding of the evo- groups, providing insights on sexual conflict lution of parental behaviour. (Chapter 9), parent–offspring conflict (Chapter 7), Since Clutton-Brock (1991) published his ency- sibling rivalry (Chapter 8), and kin-mediated clopedic bible on parental care, two new tech- cooperation (Emlen 1994, 1997). The strong link nological advances (both molecular) have helped between parental effort and mating effort (and to further invigorate parental care research. First, sexual selection patterns in general) has also driven phylogenetically based, comparative studies are the ever-growing interest in parental behaviour now commonly employed in the study of parental (Williams 1966; Trivers 1972; Emlen and Oring care. The molecular revolution has facilitated the 1977; Kokko and Jennions 2008). wide scale availability of molecular phylogenies, Parental care varies widely between species. and analysis that links behaviour to these (Good- While costly parental feeding of offspring is a near win et al. 1998). These phylogenetic studies have hallmark feature of birds and mammals, many strongly augmented and guided the more tradi- species of fishes, amphibians, and reptiles also tional behavioural ecology approach of experimen- provide care for young by simply but vigorously tal manipulation (Wright and Cuthill 1989). Second, guarding young against predators. Whether it is the the growth of genomic and bioinformatic studies mother or the father that defends the brood also has facilitated investigations into the divergence or varies widely between species. Understanding the conservation of genes, gene networks, and gene key ecological factors selecting for care and explain- regulation across species or genera that share sim- ing the plethora of parental care forms across dif- ilar behaviour. Both these new directions have been ferent taxa has remained an enduring challenge made possible because of the rapid expansion of in evolutionary behavioural ecology (Lack 1968; molecular data and because of impressive compu- Gross 2005; Kvarnemo 2010). Empirical research tational improvements that have facilitated large- has shown that providing care benefits parents by scale database creation and analysis. In general, increasing offspring survival and increasing their the molecular revolution is providing deep insights 62 978–0–19–969257–6 04-Royle-c04-drv Royle-et-al (Typeset by SPi, Chennai) 63 of 347 March 31, 2012 14:59 OUP UNCORRECTED PROOF – REVISES, 31/3/2012, SPi PATTERNS OF PARENTAL CARE IN VERTEBRATES 63 into the evolutionary and physiological mecha- and may prevent predation. However, building nisms underlying parental behaviour. such structures can be costly to the parent in In the next section, I provide an overview of terms of energy, time, and predation risk (Gau- the forms of care are generally observed across thier and Thomas 1993). Such costs are better born fishes, amphibians, reptiles, birds, and mammals by some individuals than others, and hence the and examine the factors that are thought to have nest or burrow has become much more than the selected for the evolution of viviparity and lacta- place where young are looked after and can be tion. Then I discuss the evolution of male care, thought of as an extension of the individual’s phe- female care, and biparental care as well as the evo- notype (Dawkins 1982; Soler et al. 1998). Females in lutionary transitions between these care states. I many species have been shown to prefer males that conclude the chapter with a brief overview of the build big, elaborate or particularly well-constructed patterns of parental care in humans. Whenever pos- nests (Soler et al. 1998; Östlund-Nilsson 2001). For sible, I highlight new comparative and molecular example, male penduline tits (Auriparus flaviceps) studies in order to shed light on the evolution and build complex domed nests and these nests attract maintenance of parental care and link care patterns females, and males with the largest nests are most across the different species and classes of verte- likely to mate, mate earlier, and have partners that brates. faithfully look after young (Grubbauer and Hoi 1996; Szentirmai et al. 2005, Fig. 4.1a). Female choice 4.2 Forms of care is based on nest size even when male quality and habitat quality was held constant (Grubbauer and Some researchers prefer to use the term ‘parental Hoi 1996). It turns out that the larger nests have a care’ to refer only to only post-mating behaviours better insulation capacity, thereby reducing temper- (such as care of eggs, larvae, or young after fertil- ature fluctuations and promoting embryonic devel- ization; see Chapter 1). However, some behaviours opment (Grubbauer and Hoi 1996). that occur before or during mating, such as nest In mammals, den or burrow building may have building, egg provisioning, provisioning of the evolved for purposes other than the rearing of female with nuptial gifts or courtship feeding, young (Fig. 4.1b). These year round structures that are often still regarded as parental care as they provide insulation and protection are extremely lead to higher offspring survival. Here I describe commonly used among carnivore, rodent, insec- the various forms of parental care in its broader tivore, and lagomorph species, all of whom are sense. subject to an intense predation pressure (Birks et al. 2005). For example, some species of deer mice (genus Peromyscus) build complex burrows 4.2.1 Preparation of the physical rearing that contain nest chambers, specific holes used as environment an entrance, and several long escape tunnels that The simplest form of parental care is the prepara- minimize predation. The same burrow is used for tion of a territory to receive eggs or young (Fig. both sleeping and looking after young. Recently 4.1). Species differ in terms of whether they merely behavioural experiments have mapped burrowing occupy an existing structure to receive young, behaviour onto a Peromyscus molecular phylogeny or they modify these structures, or even create to reveal consistent differences between species in new structures de novo. Regardless, the prepara- the shape and frequency of burrow making, and tion and construction of a nest, den, cavity, or bur- that species with complex burrows with many row constitutes a basic but important aspect of escape tunnels have evolved from species with sim- parental behaviour that strongly influences the sur- pler burrowing behaviour (Weber and Hoekstra vival probabilities of young (Clutton-Brock 1991). 2009). These structures provide insulation and protection Birds are without a doubt the master builders of for young from adverse environmental conditions the vertebrate world, using a diverse range of nest- (such as low temperatures, rain, or desiccation) ing materials and building nests of many different 978–0–19–969257–6 04-Royle-c04-drv Royle-et-al (Typeset by SPi, Chennai) 64 of 347 March 31, 2012 14:59 OUP UNCORRECTED PROOF – REVISES, 31/3/2012, SPi 64 THE EVOLUTION OF PARENTAL CARE Figure 4.1 Preparing for eggs and young. (a) A male Pendeline tit, (Auriparus flaviceps) with a domed shaped nests; females prefer large, well constructed nests. (b) A rabbit burrow with five kits. (c) An African weaver bird (Ploceidae) with its flask shaped nest. (d) The mud nest of a cliff swallow (Petrochelidon pyrrhonota). (e) A male three-spined stickleback (Gasterosteus aculeatus) observing a female entering his nest. (f) A male and female cichlid fish from Lake Tanganyika (Cyathopharynx furcifer) spawning in a crater nest. shapes and sizes. Most bird species build or mod- made of mud mixed with bird saliva and are shaped ify a nest in which they deposit and incubate the like pottery jugs (Fig. 4.1d). A comparative phylo- eggs. Some species build open nests (e.g. Ameri- genetic analysis of the entire swallow family reveals can robins, Turdus migratorius), others excavate a that cavity nesting and nesting in mud-made struc- cavity (e.g. downy woodpecker, Picoides pubescens), tures evolved from simple burrowing (Winkler and while some bird species simply take over the cavi- Sheldon 1993; Sheldon et al. 2005). While most bird ties made by other species lining the chamber with nests are short seasonal structures that are con- moss grass, moss, feathers, and hair to cushion the structed to protect eggs, a few bird species like eggs inside (e.g. burrowing owls, Athene cunicularia; some of the larger raptors and megapods and some Martin and Li 1992). African weaver birds (Plocei- weavers have nests that last for many years and dae) build dramatic nests that look like flasks hang- can be metres in diameter and height (Stone 1989). ing by woven loops from branches of trees.